American Journal of Botany 87(2): 243–249. 2000.
INTERACTIVE
EFFECTS OF ELEVATED
CO2
AND
TEMPERATURE ON WATER TRANSPORT IN
PONDEROSA PINE1
HAFIZ MAHERALI2
AND
EVAN H. DELUCIA
Department of Plant Biology, University of Illinois at Urbana-Champaign, 265 Morrill Hall, 505 South Goodwin Avenue,
Urbana, Illinois 61801, USA
Many studies report that water flux through trees declines in response to elevated CO2, but this response may be modified
by exposure to increased temperatures. To determine whether elevated CO2 and temperature interact to affect hydraulic
conductivity, we grew ponderosa pine seedlings for 24 wk in growth chambers with one of four atmospheric CO2 concentrations (350, 550, 750, and 1100 ppm) and either a low (158C nights, 258C days) or high (208C nights, 308C days)
temperature treatment. Vapor pressure deficits were also higher in the elevated temperature treatment. Seedling biomass
increased with CO2 concentration but was not affected by temperature. Root : shoot ratio was unaffected by CO2 and temperature. Leaf : sapwood area ratio (AL/AS) declined in response to elevated temperature but was not influenced by CO2.
Larger tracheid diameters at elevated temperature caused an increase in xylem-specific hydraulic conductivity (KS). The
increase in KS and decrease in AL/AS led to higher leaf-specific hydraulic conductivity (KL) at elevated temperature. Stomatal
conductance (gS) was correlated with KL across all treatments. Neither KS, KL, nor gS were affected by elevated CO2
concentrations. High KL in response to elevated temperature may support increased transpiration or reduce the incidence of
xylem cavitation in ponderosa pine in future, warmer climates.
Key words:
biomass allocation; CO2; hydraulic conductivity; leaf : sapwood area ratio; Pinaceae; Pinus ponderosa;
stomatal conductance; temperature; xylem anatomy.
Although there is considerable variation across studies,
in many cases growth under elevated atmospheric CO2
causes a reduction in stomatal conductance (gS) in trees
(Eamus and Jarvis, 1989; Field, Jackson, and Mooney,
1995; Curtis, 1996; Drake, Gonzàlez-Meler, and Long,
1997; Curtis and Wang, 1998). A conclusion drawn from
this observation is that water flux through trees and uptake by roots will be reduced in a future high atmospheric
CO2 climate (Eamus and Jarvis, 1989; Field, Jackson, and
Mooney, 1995; Drake, Gonzàlez-Meler, and Long, 1997).
Stomatal conductance, however, is only one control of
water flux through the soil-plant-atmosphere continuum.
Another important factor regulating water flux is water
conduction through the xylem relative to leaf area, defined as the leaf-specific hydraulic conductivity (KL; Tyree and Ewers, 1991). Leaf-specific hydraulic conductivity and leaf-level transpiration are correlated, and the role
of KL in controlling leaf water supply is well defined
(Meinzer and Grantz, 1990; Tyree and Ewers, 1991;
Sperry and Pockman, 1993). Relatively little is known
about how KL responds to elevated atmospheric CO2 in
particular and climate change in general (Saxe, Ellsworth,
and Heath, 1998). Measurements of both gS and KL in
experimental studies may provide a greater understanding
of how water flux and uptake by trees will respond to
elevated atmospheric CO2 concentrations.
Leaf-specific hydraulic conductivity is dependent on
the conducting efficiency of xylem (specific hydraulic
conductivity, KS) and the relative allocation of biomass
to xylem and leaves. Therefore, it represents the longterm effects of growth environment on plant water transport. For a shoot, KL can be expressed as
KL 5
KH
[K /A ]
5 H S
AL
[AL /AS ]
(1)
where KH is the hydraulic conductivity of a stem, AL is
the leaf area, and AS is the sapwood area. KH/AS is the
specific hydraulic conductivity of xylem (KS), and AL/AS
is the leaf : sapwood area ratio. This relationship can be
used to determine whether xylem function or biomass
allocation is the primary factor controlling water transport through the shoot. For example, at a constant KS, a
decrease in leaf area would increase KL. Higher KL permits increased transpiration without a rise in the water
potential gradient, and may be a common feature of
plants grown in environments with high evaporative demand (Tyree and Ewers, 1991; Mencuccini and Grace,
1995; Maherali, DeLucia, and Sipe, 1997).
The rise in atmospheric CO2 concentration is expected
to force a temperature increase of 1.58–4.58C in North
America (Kattenberg et al., 1996; Schimel et al., 1996).
This temperature increase will also raise the evaporative
power of the air (Gregory, Mitchell, and Brady, 1997),
as measured by the atmospheric vapor pressure deficit
(VPD). Although elevated CO2 may reduce leaf-level
transpiration (Field, Jackson, and Mooney, 1995; Drake,
Gonzàlez-Meler, and Long, 1997), exposure to high temperatures and increased evaporative demand may have
1 Manuscript received 29 January 1999; revision accepted 4 May
1999.
The authors thank T. A. Mies for maintaining the growth chambers
and C. M. Caruso and K. George for assistance with several aspects of
this research. This manuscript was improved by comments from C. M.
Caruso, A. M. Arntz, K. George, J. G. Hamilton, J. S. Hartz, S. L.
Naidu, E. L. Singsaas, and two anonymous reviewers. This research
was supported by USDA-NRI grant 94-37101-0562 and International
Arid Lands Consortium grant 96R-08.
2 Author for correspondence: e-mail: [email protected]; phone: 217244-3167; FAX: 217-244-7246.
243
244
AMERICAN JOURNAL
the opposite effect (Kolb and Robberecht, 1996). The pattern of aboveground biomass allocation, which alters KL,
varies substantially in response to CO2 concentration,
temperature, and evaporative demand (Waring and
Schlesinger, 1985; Callaway, DeLucia, and Schlesinger,
1994; Callaway et al., 1994; Margolis et al., 1995; Mencuccini and Grace, 1995; Maherali, DeLucia, and Sipe,
1997; Curtis and Wang, 1998). Elevated CO2 may also
affect xylem anatomy (Conroy et al., 1990; Tyree and
Alexander, 1993; Atkinson and Taylor, 1996; Saxe, Ellsworth, and Heath, 1998), which alters KS. The integrated
response of shoot hydraulic properties to the interaction
of elevated atmospheric CO2 and temperature is not well
understood.
To examine the interactive effects of temperature and
CO2 on tree water transport, we grew ponderosa pine
(Pinus ponderosa L.) seedlings in a four by two factorial
experiment with four levels of atmospheric CO2 and two
levels of temperature. Our objectives were to determine
(1) whether growth in elevated CO2 affects the hydraulic
conductivity and biomass allocation of ponderosa pine
and (2) whether these effects were modified by exposure
to elevated temperatures and associated increases in atmospheric evaporative demand.
METHODS
Plant material and treatment conditions—Ponderosa pine seeds of
a single half-sib family were obtained from the Institute of Forest Genetics in Placerville, California, USA. Following stratification at 48C
for 6 wk, seeds were germinated in ‘‘rootainer’’ pots (Hummert International, Earth City, Missouri, USA). After 6 wk in a greenhouse under
natural light, 80 similar-sized seedlings were transplanted into 3.14-L
PVC (polyvinyl chloride) tubes (40-cm deep) containing a mixture of
quartz sand and soil loam (10:3 v/v). The top 10-cm layer of each pot
consisted of an equal mixture of the potting soil and forest litter collected underneath a ponderosa pine stand at the Institute of Forest Genetics. Litter was applied to inoculate seedlings with appropriate mycorrhizae. Seedlings were assigned to one of eight growth chambers
with one of four atmospheric CO2 concentrations (350, 550, 750, and
1100 ppm) and either a low (158C nights, 258C days) or high (208C
nights, 308C days) temperature treatment. There were ten seedlings in
each treatment combination. Our selection of CO2 concentrations approximated projections of ;575 and ;950 ppm by years 2050 and
2100, respectively, assuming a constant 2% per year increase in anthropogenic emissions (scenario IS92-e; Schimel et al., 1996). The low
temperature treatment represents the mean minimum and maximum
growing season temperatures for ponderosa pine forests in the western
Sierra Nevada at an elevation of 1500 m. We selected elevated temperature treatment conditions based on predictions by current climate
models that forecast a maximum 4.58C increase in mean annual global
temperature (scenario IS92-e; Kattenberg et al., 1996). Because atmospheric evaporative demand and temperature covary in nature, we did
not control vapor pressure deficit independently of temperature. The low
temperature treatment provided a VPD range of 0.7–1.3 kPa, whereas
the high temperature treatment provided a VPD range of 1.3–2.4 kPa.
Our growth chambers were not designed to control absolute humidity,
therefore VPD levels were lower than that normally experienced by
ponderosa pine during the growing season in the Sierra Nevada. To
minimize a possible chamber effect, plants were rotated among chambers each week. Each set of plants experienced each chamber three
times during the experiment. Seedlings were treated with 10 g of slowrelease fertilizer (Osmocote, Sierra Chemical Co., Milpitas, California,
USA) after transfer to growth chambers and watered to field capacity
every 2 d. Seedlings were harvested after 24 wk in the growth cham-
OF
BOTANY
[Vol. 87
bers, ensuring that the majority of foliage and secondary xylem developed under treatment conditions.
Growth chambers were constructed of aluminum frames with clear
cellulose acetate walls and located inside a greenhouse room. Natural
light was supplemented with halogen lamps suspended above each
chamber to provide a 14-h photoperiod and to maintain minimum incident irradiance (photosynthetically active radiation, PAR) at the tops
of the pine seedlings above 300 mmol photons · m22 · s21. Carbon dioxide concentrations in the chambers were monitored by a SBA-1
IRGA (PP Systems, Haverhill, Massachusetts, USA). Air temperature
was measured by a sheltered, copper-constantan thermocouple suspended above the seedlings in each chamber. Relative humidity was measured with a Hygro-M1 dew-point hygrometer (General Eastern Instruments, Watertown, Massachusetts, USA). Carbon dioxide concentration
in each chamber was controlled with a custom-built relay control system
interfaced with the IRGA (infra-red gas analyzer) that permitted the
injection of pure CO2 into the growth chambers via a solonoid valve.
Air temperature was controlled using a closed loop pathway under constant cooling and controlled heat input. Chamber environmental conditions were monitored and controlled by a microcomputer running proprietary software.
Hydraulic conductivity—At harvest intact seedlings were brought to
an air-conditioned laboratory, placed underwater, and a 3–5 cm long
stem segment between the root collar and first leaf was excised and
debarked. Stem segments were placed in a waterbath for 1 h to reduce
the exudation of resin. This treatment has the effect of removing emboli
from tracheids (Lewis, Harnden, and Tyree, 1994); therefore we could
not reliably measure in situ hydraulic conductance in the seedlings.
Maximum hydraulic conductance (KH) was measured as described in
Sperry, Donnelly, and Tyree (1988). After soaking, segments were
cleared of any remaining air emboli by flushing them with a filtered
(0.2 mm) weak HCl solution (pH 5 2) under high pressure. Preliminary
experiments showed that ponderosa pine reached maximum mass flow
rate (Q, in kilograms per second) after 30 min at 170 kPa, so all segments were flushed for 1 h prior to measuring hydraulic conductance.
Measurements of KH were made at a regulated pressure of 45 kPa. Stem
efflux was collected and weighed to calculate mass flow rate.
Hydraulic conductance was defined as the mass flow rate divided by
the pressure gradient [Q/(dP/dx)]. Specific hydraulic conductivity (KS)
was calculated as KH divided by the stem area of the segment and leafspecific hydraulic conductivity (KL) was calculated as KH divided by
the leaf area of the seedling. After measuring hydraulic conductivity,
stems were perfused with filtered (0.2 mm) 0.01 basic fuschin solution
under hydrostatic pressure (;10 kPa) to determine the functional xylem
area of each segment. Dye infiltrations showed that the entire stem was
functional xylem except for a very small portion of pith. Therefore stem
cross-sectional area was considered equivalent to functional xylem or
sapwood area.
Stomatal conductance—Prior to harvest, stomatal conductance to
water vapor was measured on 3–5 seedlings per treatment combination
with a LI-1600M null-balance porometer (LI-COR, Lincoln, Nebraska,
USA) equipped with a 63.4-cm3 cylindrical cuvette (LI-1600–07). Three
measurements were made per plant. Pots were watered to field capacity
and placed in the dark for 2 h to allow plants to reach equilibrium with
soil water and then exposed to measurement conditions for 1 h. To
determine whether an intrinsic reduction (Gunderson and Wullschleger,
1994) in stomatal conductance (gS) had occurred we made measurements at common environmental conditions. Differences in gS measured
under common environmental conditions may reflect morphological
changes in stoma aperture or stomatal density. Stomatal conductance
was measured at 218C, 35% RH, an incident irradiance of 300 mmol ·
m22 · s21, and a CO2 concentration of ;425 ppm.
Xylem anatomy—Measurements of tracheid diameter and length
February 2000]
MAHERALI
AND
DELUCIA—WATER
TRANSPORT IN PONDEROSA PINE SEEDLINGS
245
were made on a subsample of stem segments used for hydraulic conductivity measurements. Stem cross sections (20 mm thick) were made
with sliding microtome (American Optical Co., Buffalo, New York,
USA) and stained with toluidine blue. We measured radial strips of cells
on sectors spaced at 908 intervals in the outermost portion of each cross
section. Fifty tracheids were measured for each stem segment. Measurements were made at 4303 with a light microscope equipped with
an ocular micrometer (Bausch and Lomb, Rochester, New York, USA).
Lumen diameter (D) was calculated as: D 5 2ab/(a 1 b), where a and
b are the short and long sides of the tracheid, respectively (Lewis and
Boose, 1995). The percentage of tracheids in 1-mm diameter classes
was calculated as in Sperry and Ikeda (1997).
Wood from the outer portions of the stem segments was used to
measure tracheid length. Several 2-cm long slivers of wood were macerated by placing them in a 1:1 solution of 10% nitric acid and 10%
chromic acid (Berlyn and Mischke, 1976). After 24 h, samples were
washed with distilled water, placed in 70% EtOH, and vortexed with 3
mm diameter glass beads. Tracheids were mounted on a slide and
stained with toluidine blue. The lengths of 35–50 tracheids per individual were measured with a light microscope and ocular micrometer as
described above.
Biomass allocation—Following harvest seedlings were separated
into roots, stems, and needles, oven dried to constant mass (608C for
48 h) in a forced-convection oven and weighed. Specific leaf area (SLA;
in centimetres squared per gram) was calculated on a subsample of
needles from each seedling. All-sided leaf area (A) for individual needles was calculated as A 5 L(C 1 2NR), where L is the needle length,
N is the number of needles per fascicle, C is the circumference of the
fascicle, and R is the fascicle radius. Leaf area per seedling was calculated as the product of SLA and leaf biomass.
Statistical analyses—Because the CO2 and temperature treatments
were not applied independently to each seedling, the plants in each
treatment combination are not true replicates (Hurlbert, 1984; Curtis
and Wang, 1998). Therefore, we treated the mean of the ten seedlings
in each treatment combination as a replicate. We used analysis of covariance (ANCOVA; Sokal and Rohlf, 1995) to determine the effects
of CO2 and temperature on total biomass, root : shoot ratio, KS, AL/AS,
KL, gS, tracheid diameter, and tracheid length. Temperature was defined
as a categorical variable and CO2 as a continuous variable in the model.
A significant temperature by CO2 interaction in the model indicates that
the slopes between a given response variable and CO2 differed across
temperature treatments. If there was no temperature by CO2 interaction
(i.e., the slopes were homogeneous) we tested for a temperature main
effect by comparing intercepts. Since responses to elevated CO2 may
be confounded by plant size, we used seedling biomass as a second
covariate in our analyses. If plant size did not have a significant effect
on the response variable, we removed it from the model. Data were log
transformed when appropriate to meet assumptions for ANCOVA. Statistical analyses were performed using Systat 5.2.1 for the Macintosh
(SPSS, Evanston, Illinois, USA).
RESULTS
Seedling biomass increased in response to elevated
CO2 (Fig. 1A; P , 0.01) and increased marginally in
response to elevated temperature (P 5 0.06). Root and
shoot biomasses increased with elevated CO2, primarily
because plants were larger in elevated CO2 (data not
shown, P , 0.05). Elevated CO2 did not directly alter the
root : shoot ratio. Although the root : shoot ratio appeared
to increase with elevated CO2 (Fig. 1B), this effect was
caused by increased seedling biomass (P , 0.05) and not
by CO2 concentration (P . 0.05). Root : shoot ratios were
also unaffected by temperature (P . 0.05). Leaf mass
Fig. 1. The effect of atmospheric CO2 concentration and air temperature on (A) total seedling biomass and (B) the root : shoot ratio for
30-wk-old ponderosa pine seedlings. Each data point is the mean of (6
1 SE) of ten seedlings.
and leaf area increased with seedling biomass (data not
shown, P , 0.01), but were not directly altered by CO2
or temperature. Sapwood area increased with seedling
biomass and elevated temperature (data not shown, P ,
0.05), but was not directly affected by CO2 concentration
(data not shown, P . 0.05)
Specific hydraulic conductivity (KS) increased in response to elevated temperature (Fig. 2A; P , 0.01), but
was not affected by elevated CO2 (P . 0.05). Leaf : sapwood (AL/AS) area ratio decreased in response to high
temperature (Fig. 2B; P , 0.05), but was not affected by
CO2 concentration. The combination of higher KS and
lower AL/AS led to increased leaf-specific hydraulic conductivity (KL) at high temperature (Fig. 2C; P , 0.01).
KL was not affected by elevated CO2 concentrations (P
246
AMERICAN JOURNAL
OF
BOTANY
[Vol. 87
Fig. 3. The effect of atmospheric CO2 concentration and air temperature on stomatal conductance (gS) for 30-wk-old ponderosa pine
seedlings. Each data point is the mean (61 SE) of 3–5 seedlings.
. 0.05). Neither KS, AL/AS, nor KL were dependent on
seedling size (data not shown, P . 0.05).
Stomatal conductance increased by 15% with elevated
temperature (Fig. 3, P , 0. 01). Although gS appeared to
decline with elevated CO2 concentrations at low temperature, this response was not statistically significant (P .
0.05). Stomatal conductance was also correlated with
leaf-specific hydraulic conductivity when expressed
across all treatments (Fig. 4).
Mean (61 SD) tracheid diameter increased significantly with elevated temperature (for high temperature,
11.51 6 0.1 mm; for low temperature, 10.06 6 0.2 mm;
Fig. 5, P , 0.05), but was unaffected by elevated CO2
concentrations (P . 0.05). Mean (61 SD) wood density
was unaffected by temperature (for high temperature,
0.42 6 0.02 g/cm2; for low temperature, 0.42 6 0.01 g/
cm2) or CO2 concentration (P . 0.05, data not shown).
DISCUSSION
Fig. 2. The effect of atmospheric CO2 concentration and air temperature on (A) specific-hydraulic conductivity (KS), (B) leaf : sapwood area ratio (AL/AS), and (C) leaf-specific hydraulic conductivity
(KL) for 30-wk-old ponderosa pine seedlings. Each data point is the
mean of (6 1 SE) of ten seedlings.
Our results suggest that elevated CO2 will have minimal effects on KS and KL, whereas elevated temperature
and atmospheric evaporative demand will increase water
transport capacity. The insensitivity of tracheid lumen diameter, and hence KS, to elevated CO2 may be common
in trees. In experiments on young saplings (#2-yr-old),
Donaldson et al. (1987) and Conroy et al. (1990) found
that elevated CO2 concentrations had no significant effect
on tracheid diameter in Pinus radiata D. Don. Atkinson
and Taylor (1996) found that elevated CO2 had no effect
on the vessel element diameter of 2-mo-old Prunus avium
L. 3 pseudocerasus Lind seedlings. Although we found
no effects of seedling size on tracheid dimension in ponderosa pine, xylem conduit dimensions are generally correlated with tree size and age (Gartner, 1995). Therefore,
tree seedlings exposed to elevated CO2 may have larger
February 2000]
MAHERALI
AND
DELUCIA—WATER
TRANSPORT IN PONDEROSA PINE SEEDLINGS
247
Fig. 5. The effect of growth in low and high air temperature on the
fraction of tracheids in 1-mm tracheid diameter classes for 30-wk-old
ponderosa pine seedlings. There were no effects of elevated CO2 concentration on tracheid diameter, so temperature data were pooled across
CO2 levels. Each data point is the mean (61 SE) of 20 seedlings (five
seedlings per treatment combination).
Fig. 4. Stomatal conductance (gS) as a function of leaf-specific hydraulic conductivity (KL) for ponderosa pine grown in one of four CO2
concentrations (350, 550, 750, and 1100 ppm) and two temperature
treatments (208C nights, 308C days; or 158C nights, 258C days). The
data were fit with least-squares regression, where gS 5 23.25 (log KL)
1 191.30, r2 5 0.52, P , 0.05. Open symbols represent plants grown
in low temperatures and closed symbols represent plants grown in high
temperatures.
tracheid or vessel diameter than control trees simply because of larger size. For example, Atkinson and Taylor
(1996) reported that 10-mo-old Quercus robur L. seedlings grown at elevated CO2 had larger vessel elements
than control trees, but could not separate the effects of
elevated CO2 from the effects of plant size and development. Size- and age-independent effects of elevated
CO2 on xylem anatomy may also become apparent with
longer term exposure (Conroy et al., 1990; Atkinson and
Taylor, 1996).
The increase in KS at high temperature was caused primarily by significantly larger tracheid lumen diameters in
seedlings grown at high temperature (Fig. 5). Because
conductance increases as a function of the fourth power
of the lumen radius, small increases in tracheid diameter
can lead to large increases in hydraulic conductance
(Zimmermann, 1983). For example, with the assumption
that tracheids are ideal capillaries, we calculated that the
14% increase in mean tracheid diameter of seedlings exposed to high vs. low temperature (Fig. 5) would drive
a 75% increase in hydraulic conductance. However, the
anatomy of bordered pits connecting adjacent tracheids
(Pothier et al., 1989) and the number of tracheids per unit
sapwood area (Atkinson and Taylor, 1996) also control
water transport in conifers. Although not measured in this
study, an increase in bordered pit permeability and tracheid numbers may have contributed to higher KS in ponderosa pine seedlings exposed to elevated temperature.
The larger tracheid diameters observed in ponderosa
pine seedlings may be caused by exposure to both elevated temperatures and VPD. Larger tracheid lumen diameter was associated with higher temperatures in Pinus
radiata (Richardson, 1964; Jenkins, 1975) and P. sylvestris (Antanova and Stasova, 1993), although these studies
did not control for VPD. Whitehead, Sheriff, and Greer
(1983) found that P. sylvestris seedlings grown in daytime VPDs of 2.0 kPa had marginally larger tracheid lumen diameters than seedlings grown in daytime VPDs of
1.0 kPa or below. We did not manipulate VPD independently from temperature; therefore we could not directly
determine whether ponderosa pine seedlings responded
specifically to high temperatures, high VPD, or to an interaction between both factors. However, transpiration is
driven primarily by VPD in conifers (Sanford and Jarvis,
1986) and is coordinated with stem hydraulic conductivity (Meinzer and Grantz, 1990; Tyree and Ewers, 1991;
Sperry and Pockman, 1993). Stem hydraulic conductivity, in turn, is dependent on xylem anatomy (Zimmermann, 1983). Thus, the most probable explanation for
larger tracheid diameter at high temperature is high VPD.
Wood hydraulic conductance and anatomical properties
were unaffected by CO2 concentration in this study,
therefore differences in KL could only occur if the AL/AS
was altered by exposure to elevated CO2. We observed
no differences in AL/AS in response to increasing CO2
concentration. Similar to our results, elevated CO2 did not
alter AL/AS in 3-yr-old P. taeda saplings grown in opentop chambers (Pataki, Oren, and Tissue, 1998). We also
found no intrinsic reduction of gS in response to elevated
CO2 (Fig. 3). Other greenhouse and open-top chamber
studies (Surano et al., 1986; Hollinger, 1987; Conroy et
al., 1988; Grulke, Homand, and Roberts, 1993; Pataki,
Oren, and Tissue, 1998) suggest that conifers may not
reduce stomatal conductance and leaf-level transpiration
in response to elevated CO2, possibly because of a general insensitivity of conifer stomata to atmospheric CO2
(Tyree and Alexander, 1993; Wang and Kellomaki, 1997;
248
AMERICAN JOURNAL
OF
BOTANY
[Vol. 87
Will and Teskey, 1997). The overall reduction of gS in
response to elevated atmospheric CO2 concentrations
across woody plant genera may also be small (Curtis and
Wang, 1998). However, because gS remained unchanged
and plant biomass increased with CO2 in our study,
whole-plant transpiration may have been higher in the
elevated CO2 treatment.
As with the response of gS in woody plants (e.g., Eamus and Jarvis, 1989; Field, Jackson, and Mooney, 1995;
Curtis, 1996; Drake, Gonzàlez-Meler, and Long, 1997;
Curtis and Wang, 1998), the effects of elevated atmospheric CO2 on KL may be variable and species-specific.
For example, Heath, Kierstens, and Tyree (1997) found
that growth in ambient 1 250 ppm CO2 concentrations
reduced KL in Quercus robur L. but not in Fagus sylvatica L. shoots. Atkinson and Taylor (1996) found that
growth in 700 ppm CO2 concentrations increased KL in
Q. robur but not in Prunus avium L. 3 pseudocerasus
stems. Our results suggest that elevated CO2 has no effect
on KL in ponderosa pine.
By combining the Penman-Montieth equation (which
describes transpiration from a forest canopy) and Darcy’s
law (which describes water transport through tree stems),
Whitehead and Jarvis (1981) developed a relationship to
predict AL/AS in response to atmospheric evaporative demand. The relationship states
trees. Because aboveground KL was correlated with gS
and hence transpiration in our study, it is possible that
root hydraulic conductivity also increased in response to
elevated temperature.
Most predictions of the response of forest ecosystems
to climate change suggest that dry-mesic forests, such as
ponderosa pine, may experience reduced water stress because of lower transpiration or enhanced water use efficiency in response to elevated CO2 (Eamus and Jarvis,
1989; Field, Jackson, and Mooney, 1995; Drake, GonzàlezMeler, and Long, 1997). Elevated CO2 did not alter KS,
AL/AS, or KL of ponderosa pine seedlings in this experiment, whereas elevated temperature increased hydraulic
conductivity. Similar to the responses observed in seedlings, mature ponderosa pine trees growing in warm and
dry climates in the field also had higher KS, lower AL/AS,
and higher KL than similar-sized trees growing in cool,
moist climates (Callaway, DeLucia, and Schlesinger,
1994; H. Maherali and E. H. DeLucia, unpublished data).
We conclude that elevated temperatures and VPD are the
primary factors influencing water transport in ponderosa
pine. A shift to a warmer, drier climate in the future may
increase tree hydraulic conductivity. This change may increase leaf-level transpiration or decrease susceptibility
to drought-induced xylem embolism, but may also reduce
leaf area development.
AL
K 3 DC
5 S
AS
VPD 3 gS
LITERATURE CITED
(2)
where nC is the water potential gradient. Based on this
relationship, AL/AS should decline in response to increased atmospheric evaporative demand. This prediction
has been supported by several studies that compared the
biomass allocation of mature trees growing in contrasting
climates (Waring, Schroeder, and Oren, 1982; Callaway,
DeLucia, and Schlesinger, 1994; Margolis et al., 1995;
Mencuccini and Grace, 1995; E. H. DeLucia, H. Maherali, and E. V. Carey, unpublished data). Our observation
that AL/AS declined in response to elevated temperature
and evaporative demand is also consistent with the
Whitehead and Jarvis (1981) theory. The combination of
increased KS and reduced AL/AS led to significantly higher
KL in seedlings grown at high temperature. High KL permits higher transpiration in response to increased evaporative demand without a rise in the water potential gradient (Tyree and Ewers, 1991; Sperry and Pockman,
1993; Mencuccini and Grace, 1995; Maherali, DeLucia,
and Sipe, 1997). Coordination between transpiration and
KL (e.g., Meinzer and Grantz, 1990; Sperry and Pockman,
1993) is also supported by the observation that KL and
gS were correlated for plants grown across all treatment
conditions (Fig. 4). High KL may reduce susceptibility to
drought-induced cavitation (Meinzer and Grantz, 1990;
Sperry and Pockman, 1993) and be an adaptive response
for ponderosa pine in xeric environments.
As in other studies (Norby, 1994; Curtis and Wang,
1998), we found that allocation to roots was not significantly affected by elevated CO2 independently of plant
size. Conifer roots may have higher hydraulic conductivity and be more vulnerable to xylem embolism than stems
(Sperry and Ikeda, 1997), suggesting that roots and stems
may play different roles in controlling water transport in
ANTONOVA, G. F., AND V. V. STASOVA. 1993. Effects of environmental
factors on wood formation in Scots pine stems. Trees 7: 214–219.
ATKINSON, C. J., AND J. M. TAYLOR. 1996. Effects of elevated CO2 on
stem growth, vessel area and hydraulic conductivity of oak and
cherry seedlings. New Phytologist 133: 617–626.
BERLYN, G. P., AND J. P. MIKSCHE. 1976. Botanical microtechnique and
cytochemistry. Iowa State University Press, Ames, Iowa, USA.
CALLAWAY, R. M., E. H. DELUCIA, AND W. H. SCHLESINGER. 1994. Biomass allocation of montane desert ponderosa pine: an analog for
response to climate change. Ecology 75: 1474–1481.
———, ———, E. M. THOMAS, AND W. H. SCHLESINGER. 1994. Compensatory responses of CO2 exchange and biomass allocation and
their effects on relative growth rate of ponderosa pine in different
CO2 and temperature regimes. Oecologia 98: 159–166.
CONROY, J. P., M. KÜPPERS, B. KÜPPERS, J. VIRGONA, AND E. W. R.
BARLOW. 1988. The influence of CO2 enrichment, phosphorus deficiency and water stress on the growth, conductance and water use
of Pinus radiata D. Don. Plant Cell and Environment 11: 91–98.
———, P. J. MILHAM, M. MAZUR, AND E. W. R. BARLOW. 1990.
Growth, dry weight partitioning and wood properties of Pinus radiata D. Don after 2 years of CO2 enrichment. Plant Cell and
Environment 13: 329–337.
CURTIS, P. S. 1996. A meta-analysis of leaf gas exchange and nitrogen
in trees grown under elevated carbon dioxide. Plant Cell and Environment 19: 127–137.
———, AND X. WANG. 1998. A meta-analysis of elevated CO2 effects
on woody plant mass, form, and physiology. Oecologia 113: 299–
313.
DONALDSON, L. A., D. HOLLINGER, T. M. MIDDLETON, AND E. D. SOUTER.
1987. Effect of CO2 enrichment on wood structure in Pinus radiata
D. Don. International Association of Wood Anatomists Bulletin 8:
285–289.
DRAKE, B. G., M. A. GONZÀLEZ-MELER, AND S. P. LONG. 1997. More
efficient plants: a consequence of rising atmospheric CO2? Annual
Review of Plant Physiology and Plant Molecular Biology 48: 609–
639.
EAMUS, D., AND P. G. JARVIS. 1989. Direct effects of increase in the
global atmospheric CO2 concentration on natural and commercial
temperate trees and forests. Advances in Ecological Research 19:
1–55.
February 2000]
MAHERALI
AND
DELUCIA—WATER
TRANSPORT IN PONDEROSA PINE SEEDLINGS
FIELD, C. B., R. B. JACKSON, AND H. A. MOONEY. 1995. Stomatal responses to increased CO2: implications from the plant to the global
scale. Plant, Cell and Environment 18: 1214–1225.
GARTNER, B. L. 1995. Patterns of xylem variation within a tree and
their hydraulic and mechanical consequences. In B. L. Gartner
[ed.], Plant stems: physiology and functional morphology, 125–
149. Academic Press, New York, New York, USA.
GREGORY, J. M., J. F. B. MITCHELL, AND A. J. BRADY. 1997. Summer
drought in northern midlatitudes in a time-dependent CO2 climate
experiment. Journal of Climate 10: 662–686.
GRULKE, N. E., J. L. HOMAND, AND S. W. ROBERTS. 1993. Physiological
adjustment of two full-sib families of ponderosa pine to elevated
CO2. Tree Physiology 12: 391–401.
GUNDERSON, C. A., AND S. D. WULLSCHLEGER. 1994. Photosynthetic
acclimation in trees to rising atmospheric CO2: a broader perspective. Photosynthesis Research 39: 369–388.
HEATH, J., G. KERSTIENS, AND M. T. TYREE. 1997. Stem hydraulic conductance of European beech (Fagus sylvatica L.) and pedunculate
oak (Quercus robur L.) grown in elevated CO2. Journal of Experimental Botany 48: 1487–1489.
HOLLINGER, D. Y. 1987. Gas exchange and dry matter allocation responses to elevation of atmospheric CO2 concentrations in seedlings of three tree species. Tree Physiology 3: 193–202.
HURLBERT, S. H. 1984. Pseudoreplication and the design of ecological
experiments. Ecological Monographs 54: 187–211.
JENKINS, P. A. 1975. Influence of temperature change on wood formation
in Pinus radiata. New Zealand Journal of Forest Science 7: 172–
191.
KATTENBERG, A., F. GIORGI, H. GRASSL, G. A. MEEHL, J. F. B. MITCHELL,
R. J. STOUFFER, T. TOKIOKA, A. J. WEAVER, AND T. M. L. WIGLEY.
1996. Global mean temperature changes for the IPCC (1992) emission scenarios. In J. T. Houghton, L. G. Meira Filho, B. A. Callender, N. Harris, A. Kattenberg, and K. Maskell [eds.], Climate
change 1995: the science of climate change, 316–324. Cambridge
University Press, New York, New York, USA.
KOLB, P. F., AND R. ROBBERECHT. 1996. High temperature and drought
stress effects on survival of Pinus ponderosa seedlings. Tree Physiology 16: 665–672.
LEWIS, A. M., AND E. R. BOOSE. 1995. Estimating volume flow rates
through xylem conduits. American Journal of Botany 82: 1112–
1116.
———, V. D. HARNDEN, AND M. T. TYREE. 1994. Collapse of waterstress emboli in the tracheids of Thuja occidentalis L. Plant Physiology 106: 1639–1646.
MAHERALI, H., E. H. DELUCIA, AND T. W. SIPE. 1997. Hydraulic adjustment of maple saplings to canopy gap formation. Oecologia
112: 472–480.
MARGOLIS, H., R. OREN, D. WHITEHEAD, AND M. R. KAUFMANN. 1995.
Leaf area dynamics of conifer forests. In W. K. Smith and T. M.
Hinckley [eds.], Ecophysiology of conifer forests, 181–223. Academic Press, New York, New York, USA.
MEINZER, F. C., AND D. A. GRANTZ. 1990. Stomatal and hydraulic conductance in growing sugarcane: stomatal adjustment to water transport capacity. Plant, Cell and Environment 13: 383–388.
MENCUCCINI, M., AND J. GRACE. 1995. Climate influences the leaf area/
sapwood area ratio in Scots pine. Tree Physiology 15: 1–10.
NORBY, R. J. 1994. Issues and perspectives for investigating root responses to elevated atmospheric carbon dioxide. Plant and Soil
165: 9–20.
PATAKI, D. E., R. OREN, AND D. T. TISSUE. 1998. Elevated carbon di-
249
oxide does not affect average canopy stomatal conductance of Pinus taeda L. Oecologia 117: 47–52.
POTHIER, D., H. A. MARGOLIS, J. POLIQUIN, AND R. H. WARING. 1989.
Relation between the permeability and anatomy of jack pine sapwood with stand development. Canadian Journal of Forest Research 19: 1564–1570.
RICHARDSON, S. D. 1964. The external environment and tracheid size
in conifers. In M. H. Zimmermann [ed.], Formation of wood in
forest trees, 367–388. Academic Press, New York, New York,
USA.
SANDFORD, A. P., AND P. G. JARVIS. 1986. Stomatal responses to humidity in selected conifers. Tree Physiology 2: 89–103.
SAXE, H., D. S. ELLSWORTH, AND J. HEATH. 1998. Tree and forest functioning in an enriched CO2 atmosphere. New Phytologist 139: 395–
436.
SCHIMEL, D., D. ALVES, I. ENTING, M. HEIMANN, F. JOOS, D. RAYNAUD,
AND T. WIGLEY. 1996. CO2 and the carbon cycle. In J. T. Houghton,
L. G. Meira Filho, B. A. Callender, N. Harris, A. Kattenberg, and
K. Maskell [eds.], Climate change 1995: the science of climate
change, 76–86. Cambridge University Press, New York, New York,
USA.
SOKAL, R. R., AND J. ROHLF. 1995. Biometry, Third Edition. W. H.
Freeman, New York, New York, USA.
SPERRY, J. S., J. R. DONNELLY, AND M. T. TYREE. 1988. A method for
measuring hydraulic conductivity and embolism in xylem. Plant,
Cell and Environment 11: 35–40.
———, AND T. IKEDA. 1997. Xylem cavitation in roots and stems of
Douglas-fir and white fir. Tree Physiology 17: 275–280.
———, AND W. T. POCKMAN. 1993. Limitations of transpiration by
hydraulic conductance and xylem cavitation in Betula occidentalis.
Plant, Cell and Environment 16: 279–287.
SURANO, K. A., P. F. DALEY, J. L. J. HOUPIS, J. H. SHINN, J. A. HELMS,
R. J. PALASSOU, AND M. P. COSTELLA. 1986. Growth and physiological responses of Pinus ponderosa (Dougl ex P. Laws.) to longterm elevated CO2 concentrations. Tree Physiology 2: 243–259.
TYREE, M. T., AND J. D. ALEXANDER. 1993. Plant water relations and
the effects of elevated CO2: a review and suggestions for future
research. Vegetatio 104/105: 47–62.
———, AND F. W. EWERS. 1991. The hydraulic architecture of trees
and other woody plants. New Phytologist 119: 345–360.
WANG, K. Y., AND S. KELLOMAKI. 1997. Stomatal conductance and
transpiration in shoots of Scots pine after 4-year exposure to elevated CO2 and temperature. Canadian Journal of Botany 75: 552–
561.
WARING, R. H., P. E. SCHROEDER, AND R. OREN. 1982. Application of
the pipe model theory to predict canopy leaf area. Canadian Journal of Forest Research 12: 556–560.
———, AND W. H. SCHLESINGER. 1985. Forest ecosystems: concepts
and management. Academic Press, New York, New York, USA.
WHITEHEAD, D., AND P. G. JARVIS. 1981. Coniferous forest and plantations. In T. T. Kozlowski [ed.], Water deficits and plant growth,
49–152. Academic Press, New York, New York, USA.
———, D. W. SHERRIFF, AND D. H. GREER. 1983. The relationship
between stomatal conductance, transpiration rate and tracheid structure in Pinus radiata clones grown at different vapour saturation
deficits. Plant, Cell and Environment 6: 703–710.
WILL, R. E., AND R. O. TESKEY. 1997. Effect of irradiance and vapour
pressure deficit on stomatal response to CO2 enrichment of four
tree species. Journal of Experimental Botany 48: 2095–2102.
ZIMMERMANN, M. H. 1983. Xylem structure and the ascent of sap.
Springer Verlag, Berlin, Germany.